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Open Access Research article

Bacterial translational regulations: high diversity between all mRNAs and major role in gene expression

Flora Picard123, Hélène Milhem4, Pascal Loubière123, Béatrice Laurent4, Muriel Cocaign-Bousquet123* and Laurence Girbal123

Author Affiliations

1 Université de Toulouse; INSA, UPS, INP; LISBP, 135 Avenue de Rangueil, Toulouse, F-31077, France

2 INRA, UMR792 Ingénierie des Systèmes Biologiques et des Procédés, Toulouse, F-31400, France

3 CNRS, UMR5504, Toulouse, F-31400, France

4 Institut de Mathématiques de Toulouse, UMR 5219, INSA de Toulouse, Université de Toulouse, 135 Avenue de Rangueil, Toulouse, F-31077, France

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BMC Genomics 2012, 13:528  doi:10.1186/1471-2164-13-528

Published: 4 October 2012

Abstract

Background

In bacteria, the weak correlations at the genome scale between mRNA and protein levels suggest that not all mRNAs are translated with the same efficiency. To experimentally explore mRNA translational level regulation at the systemic level, the detailed translational status (translatome) of all mRNAs was measured in the model bacterium Lactococcus lactis in exponential phase growth.

Results

Results demonstrated that only part of the entire population of each mRNA species was engaged in translation. For transcripts involved in translation, the polysome size reached a maximum of 18 ribosomes. The fraction of mRNA engaged in translation (ribosome occupancy) and ribosome density were not constant for all genes. This high degree of variability was analyzed by bioinformatics and statistical modeling in order to identify general rules of translational regulation. For most of the genes, the ribosome density was lower than the maximum value revealing major control of translation by initiation. Gene function was a major translational regulatory determinant. Both ribosome occupancy and ribosome density were particularly high for transcriptional regulators, demonstrating the positive role of translational regulation in the coordination of transcriptional networks. mRNA stability was a negative regulatory factor of ribosome occupancy and ribosome density, suggesting antagonistic regulation of translation and mRNA stability. Furthermore, ribosome occupancy was identified as a key component of intracellular protein levels underlining the importance of translational regulation.

Conclusions

We have determined, for the first time in a bacterium, the detailed translational status for all mRNAs present in the cell. We have demonstrated experimentally the high diversity of translational states allowing individual gene differentiation and the importance of translation-level regulation in the complex process linking gene expression to protein synthesis.

Keywords:
Translational regulation; mRNA Ribosome; Translatome; Statistical modeling; Lactococcus lactis